Imaging of the pial arterial vasculature of the human brain in vivo using high-resolution 7T time-of-flight angiography

  1. Saskia Bollmann  Is a corresponding author
  2. Hendrik Mattern
  3. Michaël Bernier
  4. Simon D Robinson
  5. Daniel J Park
  6. Oliver Speck
  7. Jonathan R Polimeni
  1. The University of Queensland, Australia
  2. Otto-von-Guericke University Magdeburg, Germany
  3. Massachusetts General Hospital, United States
  4. German Center for Neurodegenerative Diseases, Germany
  5. Harvard Medical School, United States

Abstract

The pial arterial vasculature of the human brain is the only blood supply to the neocortex, but quantitative data on the morphology and topology of these mesoscopic arteries (diameter 50-300µm) remains scarce. Because it is commonly assumed that blood flow velocities in these vessels are prohibitively slow, non-invasive time-of-flight MRI angiography (TOF-MRA)-which is well-suited to high 3D imaging resolutions-has not been applied to imaging the pial arteries. Here, we provide a theoretical framework that outlines how TOF-MRA can visualize small pial arteries in vivo, by employing extremely small voxels at the size of individual vessels. We then provide evidence for this theory by imaging the pial arteries at 140-µm isotropic resolution using a 7T MRI scanner and prospective motion correction, and show that pial arteries one voxel-width in diameter can be detected. We conclude that imaging pial arteries is not limited by slow blood flow, but instead by achievable image resolution. This study represents the first targeted, comprehensive account of imaging pial arteries in vivo in the human brain. This ultra-high-resolution angiography will enable the characterization of pial vascular anatomy across the brain to investigate patterns of blood supply and relationships between vascular and functional architecture.

Data availability

The anonymized imaging data presented in this manuscript are stored in OSF (OSF, Center for Open Science, Inc., Charlottesville, Virginia, USA) accessible via https://osf.io/nr6gc/.

The following data sets were generated

Article and author information

Author details

  1. Saskia Bollmann

    Centre for Advanced Imaging, The University of Queensland, Brisbane, Australia
    For correspondence
    saskia.bollmann@cai.uq.edu.au
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8242-8008
  2. Hendrik Mattern

    Department of Biomedical Magnetic Resonance, Otto-von-Guericke University Magdeburg, Magdeburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5740-4522
  3. Michaël Bernier

    Athinoula A Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Simon D Robinson

    Centre for Advanced Imaging, The University of Queensland, Brisbane, Australia
    Competing interests
    The authors declare that no competing interests exist.
  5. Daniel J Park

    Athinoula A Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7263-9327
  6. Oliver Speck

    German Center for Neurodegenerative Diseases, Magdeburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Jonathan R Polimeni

    Department of Radiology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1348-1179

Funding

National Institute of Biomedical Imaging and Bioengineering (P41-EB015896)

  • Jonathan R Polimeni

National Institutes of Health (S10-RR019371)

  • Jonathan R Polimeni

National Institutes of Health (S10-OD02363701)

  • Jonathan R Polimeni

European Commission (MS-fMRI-QSM 794298)

  • Simon D Robinson

National Institute of Biomedical Imaging and Bioengineering (P41-EB030006)

  • Jonathan R Polimeni

National Institute of Biomedical Imaging and Bioengineering (R01-EB019437)

  • Jonathan R Polimeni

National Institute of Neurological Disorders and Stroke (R21-NS106706)

  • Jonathan R Polimeni

National Institute of Mental Health (R01-MH111438)

  • Saskia Bollmann

National Institute of Mental Health (R01-MH111419)

  • Saskia Bollmann

Natural Sciences and Engineering Research Council of Canada

  • Michaël Bernier

Fonds de recherche du Québec – Nature et technologies

  • Michaël Bernier

Deutsche Forschungsgemeinschaft (MA 9235/1-1)

  • Hendrik Mattern
  • Oliver Speck

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Human subjects: Four healthy adults volunteered to participate in the study (four males, ages 30-46). Prior to imaging, written informed consent was obtained from the three participants scanned in Boston (Figure 5, 6, 8 and 9 and corresponding figure supplements) in accordance with the Partners Human Research Committee and the Massachusetts General Hospital Institutional Review Board (protocol #2016P000274); after the study completion, a consent form addendum was used to obtain informed consent from each participant specifically to share their anonymized data on a public data repository. For the single subject from Magdeburg (Figure 7 and corresponding figure supplements) the consent to share openly the data in anonymized form was acquired prospectively (facultative option in study consent form) in accordance with the 'Ethikkommission Otto-von-Guericke-Universität Magdeburg' (protocol 15/20).

Reviewing Editor

  1. Saad Jbabdi, University of Oxford, United Kingdom

Publication history

  1. Preprint posted: June 10, 2021 (view preprint)
  2. Received: June 11, 2021
  3. Accepted: April 28, 2022
  4. Accepted Manuscript published: April 29, 2022 (version 1)
  5. Version of Record published: May 30, 2022 (version 2)

Copyright

© 2022, Bollmann et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Saskia Bollmann
  2. Hendrik Mattern
  3. Michaël Bernier
  4. Simon D Robinson
  5. Daniel J Park
  6. Oliver Speck
  7. Jonathan R Polimeni
(2022)
Imaging of the pial arterial vasculature of the human brain in vivo using high-resolution 7T time-of-flight angiography
eLife 11:e71186.
https://doi.org/10.7554/eLife.71186
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